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Diversity Among Potato Virus Y Isolates Obtained from Potatoes Grown in the United States

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Diversity Among Potato Virus Y Isolates Obtained from Potatoes Grown in the United States Virology Diversity Among Potato virus Y Isolates Obtained from Potatoes Grown in the United States L. M. Piche, R. P. Singh, X. Nie, and N. C. Gudmestad First and fourth authors: Department of Plant Pathology, North Dakota State University, Fargo 58105; and second and third authors: Potato Research Centre, Agriculture and Agri-Food Canada, P.O. Box 20280, Fredericton, NB, Canada E3B 4Z7. Accepted for publication 2 September 2004. ABSTRACT Piche, L. M., Singh, R. P., Nie, X., and Gudmestad, N. C. 2004. Diversity appear in high frequency. In contrast to European experiences, PVY tuber among Potato virus Y isolates obtained from potatoes grown in the United necrosis isolates have a PVYO coat protein rather than that of PVYN. States. Phytopathology 94:1368-1375. Several PVYN:O recombinant isolates induced potato tuber necrotic ring- spot disease (PTNRD) in the highly susceptible potato cv. Yukon Gold. Potato field isolates (Solanum tuberosum) of Potato virus Y (PVY) The PTNRD symptoms produced by these PVYN:O recombinants were collected from the midwestern and western United States were charac- atypical compared with lesions found on the same cultivar infected with terized using serological, molecular, and biological assays. PVY field either the European or North American PVYNTN isolates. These PVYN:O isolates were grouped into the previously defined categories: PVYO, isolates produced a roughly circular, sunken necrotic lesion on the surface European PVYNTN, North American PVYNTN, and PVYN:O recombinant of the tuber instead of the typical external sunken ring pattern displayed and four previously undefined groups. Studies reported here agree with by PVYNTN isolates. This study establishes the complex nature of PVY published reports from Europe and elsewhere in North America as PVY populations within the U.S. potato industry and clearly demonstrates the isolates capable of causing veinal necrosis in tobacco indicator plants diverse nature of PVY in the United States. Potato virus Y (PVY) belongs to the largest plant virus family, appearance of external rings on the surface of tubers. Initially Potyviridae. The most common PVY strains affecting potatoes are these rings protrude, later becoming sunken and necrotic with differentiated by reaction on potato (Solanum tuberosum L.) and symptoms growing more pronounced during storage. The disease tobacco (Nicotiana tabacum L.). Several strains of PVY are reduces tuber quality, with the necrotic symptoms rendering known. PVYO (the “ordinary” strain) is ubiquitous among potato affected tubers unsuitable for fresh market, processing, or seed. A production areas, causing mild to severe mosaic symptoms, de- major difficulty in screening for PVY isolates that cause tuber pending on the cultivar. This PVY strain was first classified in necrosis is that they cannot be distinguished from PVYN using 1931 (31) and has recently become epidemic throughout the current serological methods (33,34). United States (7). The widespread nature of PVY may be largely More recently, isolates resembling PVYN in tobacco, which are due to potato cultivars being grown that do not express symptoms serologically related to PVYO, have been reported. For instance, of the disease, compromising seed certification and regulatory PVYN-Wilga was first described in 1991 in Europe, along with inspections (7). PVYC induces stipple streak symptoms in potato isolates I-L56 and I-136, both isolated in 1992 in North America cultivars bearing the Nc gene. PVYZ overcomes resistance genes (3,18,19). Analysis of nucleotide sequences of PVYN-Wilga and effective against both PVYO and PVYC (10,12). European (Eu) PVYNTN indicates that both are recombinant iso- In the 1950s, a new tobacco veinal necrosis strain of PVY lates, with a genome comprised of segments from PVYO and Eu (PVYN) was found in Europe and South America and has since PVYNTN (8). By targeting three major recombinant junctions spread worldwide, eventually being detected in North America in in the genome of Eu PVYNTN, a multiplex reverse transcrip- 1990 (15,28). PVYN is frequently symptomless or produces mild tion-polymerase chain reaction (RT-PCR) assay was developed to severe mosaic symptoms in potatoes along with severe veinal (22). Separate primer pairs were designed to bind to the re- necrosis and leaf death in tobacco. Nonetheless, several reports combinant junctions located at the HC/Pro-P3 gene region, the have associated PVYN with yield and quality losses in resistant or 6K2-NIa gene region, and the C-terminal region of the coat symptomless potatoes (7,9). A variant of PVYN, termed PVYNTN, protein (CP) gene (22). Recombinant isolates sharing a PVYO includes isolates that cause potato tuber necrotic ringspot disease coat protein have become common in certain regions of North (PTNRD) and belong to the necrotic group (N) of PVY based on America and are presently referred to as PVYN:O (5,25,30). In the serology and the ability to induce veinal necrosis symptoms in absence of full-length sequences, only one recombination tobacco (13,35). PVYNTN was first observed in Hungary in the late junction site has been found to exist in PVYN:O isolates at the 1970s (1), and more recently in many potato production areas HC/Pro-P3 region using the multiplex RT-PCR assay (22). worldwide, including North America in 1993 (16). PVYNTN iso- The PVYN:O recombinant isolates studied so far, along with lates can cause severe chlorotic mosaic symptoms on potato PVYN-Wilga, have not been shown to induce tuber necrosis leaves in addition to PTNRD. PTNRD is characterized by the symptoms in potato (22,30). The diagnosis of tuber necrosis-inducing isolates of PVY has become difficult due to the increasing numbers of recognized Corresponding author: N. C. Gudmestad E-mail address: [email protected] isolates and the incidence of mixed infections. Numerous efforts have been initiated to characterize PVY isolates using an RT-PCR Publication no. P-2004-1018-02R assay targeting specific areas of the genome (2,20,21,36). The P1 © 2004 The American Phytopathological Society gene region has been proposed to be the least conserved region 1368 PHYTOPATHOLOGY among potyviruses (6) and also within strains of PVY (14). An antibody 1F5 is specific for PVYN (PN 26001). A Potato virus X RT-PCR assay, based on sequence variation within the P1 gene, (PVX) ELISA (PN 10000) also was conducted to rule out has allowed PVY isolates to be initially categorized as either synergistic interactions, which could result in necrotic symptoms PVYO or PVYN/NTN (21), allowing the potential PTNRD-inducing in tobacco bioassays (29). All reagents were obtained from Agdia, isolates to be separated from innocuous PVYO isolates. This and the assays were carried out in triplicate according to manu- duplex RT-PCR assay also will detect mixed infections of several facturer’s instructions. Samples were considered positive if they PVY pathotypes but not differentiate a mixed infection of several produced an absorbance value twice the standard deviation of the isolates of the same pathotype. A subsequent RT-PCR assay tar- healthy control. geting three major recombination junctions allows further separa- Total RNA extraction. Total RNA was extracted either from tion of PVYN/NTN isolates into recombinant, such as Eu PVYNTN; original potato leaf or tuber tissue or from infected tobacco leaf nonrecombinant, represented by North American PVYNTN (NA tissue with the RNeasy Plant Mini Kit (Qiagen, Valencia, CA). PVYNTN); and PVYN:O recombinant isolates (22). Leaf and tuber tissue were ground in liquid nitrogen with an The objective of this study was to characterize and differentiate oven-baked (240°C for 4 h) sterilized mortar and pestle. A sample field isolates obtained from various potato production regions in of the powdered tissue (approximately 100 mg) was extracted for the United States. Further, we wanted to assess the PVY popu- total RNA according to the manufacturer’s instructions. Total lation and to determine the frequency with which isolates group RNA was eluted in 50 µl of RNase-free water and centrifuged for into the current classification of PVY strains based on a combina- 1 min at 8,000 × g. The resulting RNA was stored at –80°C. tion of enzyme-linked immunosorbent assay (ELISA), RT-PCR, RT-PCR. Four microliters of concentrated total RNA extract and bioassays, and to determine the extent and relative impor- was diluted with 6 µl of RNase-free water to reduce nonspecific tance of PTNRD-producing isolates. amplification (30), incubated at 65°C for 8 min, and chilled on ice for 3 min. To the denatured RNA extract, 15 µl of RT reaction MATERIALS AND METHODS mixture (1× M-MLV RT Buffer [Promega, Madison, WI], 1.5 mM each dNTP [Roche, Indianapolis, IN], 20 units of RNasin [Pro- PVY isolates. A total of 193 tuber and leaf samples were mega], 1 µM Random Hexamers [Applied Biosystems, Foster collected from fields originating in Idaho (ID), Minnesota (MN), City, CA], and 200 units of M-MLV reverse transcriptase [Pro- North Dakota (ND), Nebraska (NE), Nevada (NV), Oregon (OR), mega]) was added to provide a final volume of 25 µl. Samples and Texas (TX), during 2001 to 2003. Samples were generally were incubated at 42°C for 1 h followed by 95°C for 3 min to collected by one of the authors or at their request (N. C. terminate the RT reaction. The resulting cDNA was stored at Gudmestad). Leaf samples submitted to our laboratory of un- –20°C. known origin were labeled “Unk”. All original samples were Separate duplex, triplex, and recombinant point RT-PCRs were tested initially using serological and RT-PCR assays and then carried out using primer sequences and reaction conditions previ- stored as freeze-dried leaf tissue at −80°C. Of the 193 original ously reported (21,22). Duplex PCR for distinguishing PVYO samples, 58 were further selected based on serological properties, from PVYN/NTN isolates was performed using 5 µl of cDNA molecular analysis, and representative geographic region to be mixture in a final volume of 25 µl containing 1× PCR Buffer multiplied in tobacco cv.
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